Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1983 Oct 1;97(4):957–962. doi: 10.1083/jcb.97.4.957

Changes in the basement membrane zone components during skeletal muscle fiber degeneration and regeneration

PMCID: PMC2112627  PMID: 6225786

Abstract

The basement membrane of skeletal muscle fibers is believed to persist unchanged during myofiber degeneration and act as a tubular structure within which the regeneration of new myofibers occurs. In the present study we describe macromolecular changes in the basement membrane zone during muscle degeneration and regeneration, as monitored by immunofluorescence using specific antibodies against types IV and V collagen, laminin, and heparan sulfate proteoglycan and by the binding of concanavalin A (Con A). Skeletal muscle regeneration was induced by autotransplantation of the extensor digitorum longus muscle in rats. After this procedure, the myofibers degenerate; this is followed by myosatellite cell activation, proliferation, and fusion, resulting in the formation of new myotubes that mature into myofibers. In normal muscle, the distribution of types IV and V collagen, laminin, heparan sulfate proteoglycan, and Con A binding was seen in the pericellular basement membrane region. In autotransplanted muscle, the various components of the basement membrane zone disappeared, leaving behind some unidentifiable component that still bound Con A. Around the regenerated myotubes a new basement membrane (zone) reappeared, which persisted during maturation of the regenerating muscle. The distribution of various basement membrane components in the regenerated myofibers was similar to that seen in the normal muscle. Based on our present and previous study (Gulati, A.K., A.H. Reddi, and A.A. Zalewski, 1982, Anat. Rec. 204:175-183), it appears that some of the original basement membrane zone components disappear during myofiber degeneration and initial regeneration. As a new basement membrane develops, its components reappear and persist in the mature myofibers. We conclude that skeletal muscle fiber basement membrane (zone) is not a static structure as previously thought, but rather that its components change quite rapidly during myofiber degeneration and regeneration.

Full Text

The Full Text of this article is available as a PDF (2.3 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allbrook D. Skeletal muscle regeneration. Muscle Nerve. 1981 May-Jun;4(3):234–245. doi: 10.1002/mus.880040311. [DOI] [PubMed] [Google Scholar]
  2. Beach R. L., Burton W. V., Hendricks W. J., Festoff B. W. Extracellular matrix synthesis by skeletal muscle in culture. Proteins and effect of enzyme degradation. J Biol Chem. 1982 Oct 10;257(19):11437–11442. [PubMed] [Google Scholar]
  3. Burden S. J., Sargent P. B., McMahan U. J. Acetylcholine receptors in regenerating muscle accumulate at original synaptic sites in the absence of the nerve. J Cell Biol. 1979 Aug;82(2):412–425. doi: 10.1083/jcb.82.2.412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carlson B. M. A review of muscle transplantation in mammals. Physiol Bohemoslov. 1978;27(5):387–400. [PubMed] [Google Scholar]
  5. Carlson B. M., Gutmann E. Regneration in free grafts of normal and denervated muscles in the rat: morphology and histochemistry. Anat Rec. 1975 Sep;183(1):47–62. doi: 10.1002/ar.1091830106. [DOI] [PubMed] [Google Scholar]
  6. Courtoy P. J., Timpl R., Farquhar M. G. Comparative distribution of laminin, type IV collagen, and fibronectin in the rat glomerulus. J Histochem Cytochem. 1982 Sep;30(9):874–886. doi: 10.1177/30.9.7130672. [DOI] [PubMed] [Google Scholar]
  7. Duance V. C., Restall D. J., Beard H., Bourne F. J., Bailey A. J. The location of three collagen types in skeletal muscle. FEBS Lett. 1977 Jul 15;79(2):248–252. doi: 10.1016/0014-5793(77)80797-7. [DOI] [PubMed] [Google Scholar]
  8. Ekblom P. Formation of basement membranes in the embryonic kidney: an immunohistological study. J Cell Biol. 1981 Oct;91(1):1–10. doi: 10.1083/jcb.91.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Foidart J. M., Bere E. W., Jr, Yaar M., Rennard S. I., Gullino M., Martin G. R., Katz S. I. Distribution and immunoelectron microscopic localization of laminin, a noncollagenous basement membrane glycoprotein. Lab Invest. 1980 Mar;42(3):336–342. [PubMed] [Google Scholar]
  10. Foidart J. M., Reddi A. H. Immunofluorescent localization of type IV collagen and laminin during endochondral bone differentiation and regulation by pituitary growth hormone. Dev Biol. 1980 Mar;75(1):130–136. doi: 10.1016/0012-1606(80)90149-9. [DOI] [PubMed] [Google Scholar]
  11. Furcht L. T., Wendelschafer-Crabb G., Woodbridge P. A. Cell surface changes accompanying myoblast differentiation. J Supramol Struct. 1977;7(3-4):307–322. doi: 10.1002/jss.400070305. [DOI] [PubMed] [Google Scholar]
  12. Gay S., Martinez-Hernandez A., Rhodes R. K., Miller E. J. The collagenous exocytoskeleton of smooth muscle cells. Coll Relat Res. 1981 Jul;1(4):377–384. doi: 10.1016/s0174-173x(81)80014-3. [DOI] [PubMed] [Google Scholar]
  13. Grant M. E., Heathcote J. G., Orkin R. W. Current concepts of basement-membrane structure and function. Biosci Rep. 1981 Nov;1(11):819–842. doi: 10.1007/BF01114816. [DOI] [PubMed] [Google Scholar]
  14. Gulati A. K., Reddi A. H., Zalewski A. A. Distribution of fibronectin in normal and regenerating skeletal muscle. Anat Rec. 1982 Nov;204(3):175–183. doi: 10.1002/ar.1092040302. [DOI] [PubMed] [Google Scholar]
  15. Gulati A. K., Zalewski A. A. Muscle allograft survival after cyclosporin A immunosuppression. Exp Neurol. 1982 Aug;77(2):378–385. doi: 10.1016/0014-4886(82)90251-5. [DOI] [PubMed] [Google Scholar]
  16. Gulati A. K., Zalewski A. A., Reddi A. H. An immunofluorescent study of the distribution of fibronectin and laminin during limb regeneration in the adult newt. Dev Biol. 1983 Apr;96(2):355–365. doi: 10.1016/0012-1606(83)90173-2. [DOI] [PubMed] [Google Scholar]
  17. Hansen-Smith F. M., Carlson B. M. Cellular responses to free grafting of the extensor digitorum longus muscle of the rat. J Neurol Sci. 1979 Apr;41(2):149–173. doi: 10.1016/0022-510x(79)90035-2. [DOI] [PubMed] [Google Scholar]
  18. Hassell J. R., Robey P. G., Barrach H. J., Wilczek J., Rennard S. I., Martin G. R. Isolation of a heparan sulfate-containing proteoglycan from basement membrane. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4494–4498. doi: 10.1073/pnas.77.8.4494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kanwar Y. S., Farquhar M. G. Isolation of glycosaminoglycans (heparan sulfate) from glomerular basement membranes. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4493–4497. doi: 10.1073/pnas.76.9.4493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kefalides N. A., Alper R., Clark C. C. Biochemistry and metabolism of basement membranes. Int Rev Cytol. 1979;61:167–228. doi: 10.1016/s0074-7696(08)61998-1. [DOI] [PubMed] [Google Scholar]
  21. Kühl U., Timpl R., von der Mark K. Synthesis of type IV collagen and laminin in cultures of skeletal muscle cells and their assembly on the surface of myotubes. Dev Biol. 1982 Oct;93(2):344–354. doi: 10.1016/0012-1606(82)90122-1. [DOI] [PubMed] [Google Scholar]
  22. Laurie G. W., Leblond C. P., Martin G. R. Localization of type IV collagen, laminin, heparan sulfate proteoglycan, and fibronectin to the basal lamina of basement membranes. J Cell Biol. 1982 Oct;95(1):340–344. doi: 10.1083/jcb.95.1.340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Liotta L. A., Goldfarb R. H., Brundage R., Siegal G. P., Terranova V., Garbisa S. Effect of plasminogen activator (urokinase), plasmin, and thrombin on glycoprotein and collagenous components of basement membrane. Cancer Res. 1981 Nov;41(11 Pt 1):4629–4636. [PubMed] [Google Scholar]
  24. Martinez-Hernandez A., Gay S., Miller E. J. Ultrastructural localization of type V collagen in rat kidney. J Cell Biol. 1982 Feb;92(2):343–349. doi: 10.1083/jcb.92.2.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Martinez-Hernandez A., Marsh C. A., Clark C. C., Macarak E. J., Brownell A. G. Fibronectin: its relationship to basement membranes. II. Ultrastructural studies in rat kidney. Coll Relat Res. 1981 Sep;1(5):405–418. doi: 10.1016/s0174-173x(81)80025-8. [DOI] [PubMed] [Google Scholar]
  26. McMahan U. J., Sanes J. R., Marshall L. M. Cholinesterase is associated with the basal lamina at the neuromuscular junction. Nature. 1978 Jan 12;271(5641):172–174. doi: 10.1038/271172a0. [DOI] [PubMed] [Google Scholar]
  27. Peltonen L., Myllylä R., Tolonen U., Myllylä V. V. Changes in collagen metabolism in diseased muscle. II. Immunohistochemical studies. Arch Neurol. 1982 Dec;39(12):756–759. doi: 10.1001/archneur.1982.00510240018005. [DOI] [PubMed] [Google Scholar]
  28. Pena S. D., Gordon B. B., Karpati G., Carpenter S. Lectin histochemistry of human skeletal muscle. J Histochem Cytochem. 1981 Apr;29(4):542–546. doi: 10.1177/29.4.6166659. [DOI] [PubMed] [Google Scholar]
  29. Rao C. N., Margulies I. M., Tralka T. S., Terranova V. P., Madri J. A., Liotta L. A. Isolation of a subunit of laminin and its role in molecular structure and tumor cell attachment. J Biol Chem. 1982 Aug 25;257(16):9740–9744. [PubMed] [Google Scholar]
  30. Risteli L., Risteli J. Basement membrane research. Med Biol. 1981 Aug;59(4):185–189. [PubMed] [Google Scholar]
  31. Rojkind M., Ponce-Noyola P. The extracellular matrix of the liver. Coll Relat Res. 1982 Mar;2(2):151–175. doi: 10.1016/s0174-173x(82)80031-9. [DOI] [PubMed] [Google Scholar]
  32. Roll F. J., Madri J. A., Albert J., Furthmayr H. Codistribution of collagen types IV and AB2 in basement membranes and mesangium of the kidney. an immunoferritin study of ultrathin frozen sections. J Cell Biol. 1980 Jun;85(3):597–616. doi: 10.1083/jcb.85.3.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sanes J. R., Cheney J. M. Lectin binding reveals a synapse-specific carbohydrate in skeletal muscle. Nature. 1982 Dec 16;300(5893):646–647. doi: 10.1038/300646a0. [DOI] [PubMed] [Google Scholar]
  34. Sanes J. R. Laminin, fibronectin, and collagen in synaptic and extrasynaptic portions of muscle fiber basement membrane. J Cell Biol. 1982 May;93(2):442–451. doi: 10.1083/jcb.93.2.442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schmalbruch H. The morphology of regeneration of skeletal muscles in the rat. Tissue Cell. 1976;8(4):673–692. doi: 10.1016/0040-8166(76)90039-2. [DOI] [PubMed] [Google Scholar]
  36. Spiro R. G. Nature of the glycoprotein components of basement membranes. Ann N Y Acad Sci. 1978 Jun 20;312:106–121. doi: 10.1111/j.1749-6632.1978.tb16796.x. [DOI] [PubMed] [Google Scholar]
  37. Stenman S., Vaheri A. Distribution of a major connective tissue protein, fibronectin, in normal human tissues. J Exp Med. 1978 Apr 1;147(4):1054–1064. doi: 10.1084/jem.147.4.1054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Timpl R., Rohde H., Robey P. G., Rennard S. I., Foidart J. M., Martin G. R. Laminin--a glycoprotein from basement membranes. J Biol Chem. 1979 Oct 10;254(19):9933–9937. [PubMed] [Google Scholar]
  39. Vracko R. Basal lamina layering in diabetes mellitus. Evidence for accelerated rate of cell death and cell regeneration. Diabetes. 1974 Feb;23(2):94–104. [PubMed] [Google Scholar]
  40. Vracko R. Basal lamina scaffold-anatomy and significance for maintenance of orderly tissue structure. Am J Pathol. 1974 Nov;77(2):314–346. [PMC free article] [PubMed] [Google Scholar]
  41. Vracko R., Benditt E. P. Basal lamina: the scaffold for orderly cell replacement. Observations on regeneration of injured skeletal muscle fibers and capillaries. J Cell Biol. 1972 Nov;55(2):406–419. doi: 10.1083/jcb.55.2.406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Vracko R., Benditt E. P. Capillary basal lamina thickening. Its relationship to endothelial cell death and replacement. J Cell Biol. 1970 Oct;47(1):281–285. doi: 10.1083/jcb.47.1.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Yaoita H., Foidart J. M., Katz S. I. Localization of the collagenous component in skin basement membrane. J Invest Dermatol. 1978 Apr;70(4):191–193. doi: 10.1111/1523-1747.ep12541313. [DOI] [PubMed] [Google Scholar]
  44. Zimmermann B., Merker H. J., Barrach H. J. Basement membrane alterations after treatment with trypsin, hyaluronidase or collagenase. Virchows Arch B Cell Pathol Incl Mol Pathol. 1982;40(1):9–15. doi: 10.1007/BF02932846. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES